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Chapter 15 : Are You Out There? Intercellular Signaling in the Microbial World

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Abstract:

This chapter emphasizes recurring themes in bacterial signaling. Bacterial metabolites include N-acyl-L-homoserine lactones (AHL) first discovered in and produced by various gram-negative bacteria, furanosyl borate diester (AI-2) first discovered in Vibrio harveyi and produced by a diverse range of bacteria, signaling peptides produced by many gram-positive bacteria, butyrolactones produced by species and 3-hydroxypalmitic acid methyl ester (PAME) produced by . The cell density sensing or "quorum sensing" hypothesis proposes that the concentration of an intercellular signal, produced by a growing population and accumulating in the surrounding extracellular environment, is proportional to the cell density of that population. The rationale is that the plant immune system, which responds to tissue damage, is not capable of resolving infections at this cell density. The chapter discusses the implications of intercellular signaling mechanism (ISM)-regulated coordinated behaviors on three levels. First, it considers how intercellular signaling within species can extend the range of phenotypes and niches available to bacteria at the cost of adaptive flexibility. Second, it appraises the evidence for intercellular signaling between species in mixed communities and considers its potential impact on microbial community dynamics. Third, it considers how bacterial ISMs may be exploited by higher organisms in interdomain interactions.

Citation: Manefield M, Turner S, Lilley A, Bailey M. 2004. Are You Out There? Intercellular Signaling in the Microbial World, p 231-248. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch15

Key Concept Ranking

Microbial Ecology
0.90474427
Bacterial Diseases
0.6765939
Furanosyl Borate Diester
0.56060606
Gram-Negative Bacteria
0.4490878
Gram-Positive Bacteria
0.4415401
Horizontal Gene Transfer
0.41804934
0.90474427
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Figures

Image of FIGURE 1
FIGURE 1

Structures of well-characterized signaling molecules. (A) -3-oxohexonoyl-L-homoserine lactone (OHHL), which regulates expression of bioluminescence in . (B) Furanosyl borate diester (AI-2), which regulates expression of bioluminescence in . (C) A γ-butyrolactone (A-factor), which regulates antibiotic production in . (D) Amino acid sequences of peptide signals. In the order listed they are AIF, which regulates antibiotic production in ; cAD1, which regulates conjugation in ; ComX, which regulates competence in ; and CSF, which regulates competence in . (E) PAME, which regulates virulence factor production in . (F) A halogenated furanone produced by the red marine macroalga that acts as an AHL antagonist.

Citation: Manefield M, Turner S, Lilley A, Bailey M. 2004. Are You Out There? Intercellular Signaling in the Microbial World, p 231-248. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch15
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Image of FIGURE 2
FIGURE 2

-Acyl-L-homoserine lactone (AHL)-mediatcd gene expression in . The gene encodes the AHL synthase protein LuxI. AHLs diffuse across cellular membranes. Above a certain concentration AHLs bind to the LuxR signal receptor protein (encoded by the gene) which activates transcription of target (structural) genes, thereby expressing the signaling regulated phenotype. In the case of the marine symbiont the specific AHL is -3-oxohexonoyl-L-homoserine lactone and the structural genes are those encoding luminescence ().

Citation: Manefield M, Turner S, Lilley A, Bailey M. 2004. Are You Out There? Intercellular Signaling in the Microbial World, p 231-248. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch15
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Image of FIGURE 3
FIGURE 3

Theoretical, diagrammatic representation of the accumulation of intercellular signals in different environments. The ratio of signal molecules (black dots) to cells (grey ovals) is constant in each frame. Target gene expression occurs when signal concentrations in each cell reach a certain level (for example, eight black dots per cell). (A) A single cell producing a diffusible metabolite with no external limitation to diffusion (a planktonic marine cell for example). (B) A population of cells producing a diffusible metabolite with no external limitation to diffusion (a floc for example). (C) A single cell producing a diffusible metabolite with diffusion limited by the surface to which it is attached (on a marine surface for example). (D) A single cell producing a diffusible metabolite with diffusion limited by the space in which the cell is confined (a light organ or xylem for example).

Citation: Manefield M, Turner S, Lilley A, Bailey M. 2004. Are You Out There? Intercellular Signaling in the Microbial World, p 231-248. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch15
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Image of FIGURE 4
FIGURE 4

The importance of cell density related to a bacterial growth curve (diamonds). (A) The traditional view of cell density sensing, known as quorum sensing, suggests that ISMs have evolved to induce gene expression at a specific cell density, e.g., at an optical density of 7 (arrow). (B) An alternative view of cell density sensing suggests that ISMs have evolved to prevent gene expression at low cell densities when resources are best utilized for primary functions, such as cell division, rather than secondary functions, such as antibiotic or exoenzyme production. The intensity of the shading represents evolution's insatiable demand for replication, which is imagined to abate as cell numbers increase. The intensity of shading, therefore, also inversely represents the availability of resources for the expression of auxiliary phenotypes. This model, in which ISMs are not required to identify specific cell densities, is consistent with the disruptive influence of environmental parameters on the fidelity of the cell-density-sensing mechanism.

Citation: Manefield M, Turner S, Lilley A, Bailey M. 2004. Are You Out There? Intercellular Signaling in the Microbial World, p 231-248. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch15
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Image of FIGURE 5
FIGURE 5

Distribution of distinct intercellular signaling mechanisms throughout the bacteria. AHLs have only been found in the α, β, and γ classes of the phylum Proteobacteria. Peptide- and butyrolactone-based signaling systems have only been found in the phylum Firmicutes. PAME has only been found in the genus .

Citation: Manefield M, Turner S, Lilley A, Bailey M. 2004. Are You Out There? Intercellular Signaling in the Microbial World, p 231-248. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch15
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Image of FIGURE 6
FIGURE 6

Neighbor-joining phylogeny of LuxR homologues with sequence clusters shaded according to taxonomic grouping: alphaproteobacteria, grey: betaprotcobacteria, square cross-hatching; and gammaproteobacteria, light and heavy spp.) diagonal lines. Known functional AHL receptors are labeled and indicated by solid lines. Sequences that have-only been identified by sequence homology are indicated by dotted lines. Bootstrap support (>60%) is indicated. Asterisk denotes sequence.

Citation: Manefield M, Turner S, Lilley A, Bailey M. 2004. Are You Out There? Intercellular Signaling in the Microbial World, p 231-248. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch15
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References

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Tables

Generic image for table
TABLE 1

Phylogenetic association of proteobacterial AHL systems

Citation: Manefield M, Turner S, Lilley A, Bailey M. 2004. Are You Out There? Intercellular Signaling in the Microbial World, p 231-248. In Miller R, Day M (ed), Microbial Evolution. ASM Press, Washington, DC. doi: 10.1128/9781555817749.ch15

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